MBE Advance Access originally published online on July 28, 2004
Molecular Biology and Evolution 2004 21(11):2130-2139; doi:10.1093/molbev/msh223
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Research Article |
Molecular Evolution of Sex-Biased Genes in Drosophila
Department of Biology II, Section of Evolutionary Biology, University of Munich (LMU), Munich, Germany
E-mail: parsch{at}zi.biologie.uni-muenchen.de.
Studies of morphology, interspecific hybridization, protein/DNA sequences, and levels of gene expression have suggested that sex-related characters (particularly those involved in male reproduction) evolve rapidly relative to non–sex-related characters. Here we report a general comparison of evolutionary rates of sex-biased genes using data from cDNA microarray experiments and comparative genomic studies of Drosophila. Comparisons of nonsynonymous/synonymous substitution rates (dN/dS) between species of the D. melanogaster subgroup revealed that genes with male-biased expression had significantly faster rates of evolution than genes with female-biased or unbiased expression. The difference was caused primarily by a higher dN in the male-biased genes. The same pattern was observed for comparisons among more distantly related species. In comparisons between D. melanogaster and D. pseudoobscura, genes with highly biased male expression were significantly more divergent than genes with highly biased female expression. In many cases, orthologs of D. melanogaster male-biased genes could not be identified in D. pseudoobscura through a Blast search. In contrast to the male-biased genes, there was no clear evidence for accelerated rates of evolution in female-biased genes, and most comparisons indicated a reduced rate of evolution in female-biased genes relative to unbiased genes. Male-biased genes did not show an increased ratio of nonsynonymous/synonymous polymorphism within D. melanogaster, and comparisons of polymorphism/divergence ratios suggest that the rapid evolution of male-biased genes is caused by positive selection.
Key Words: codon bias • comparative genomics • gene expression • sexual selection
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  N. Derome, B. Bougas, S. M. Rogers, A. R. Whiteley, A. Labbe, J. Laroche, and L. Bernatchez Pervasive Sex-Linked Effects on Transcription Regulation As Revealed by Expression Quantitative Trait Loci Mapping in Lake Whitefish Species Pairs (Coregonus sp., Salmonidae) Genetics, August 1, 2008; 179(4): 1903 - 1917. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. F. Baines, S. A. Sawyer, D. L. Hartl, and J. Parsch Effects of X-Linkage and Sex-Biased Gene Expression on the Rate of Adaptive Protein Evolution in Drosophila Mol. Biol. Evol., August 1, 2008; 25(8): 1639 - 1650. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Llopart and J. M. Comeron Recurrent Events of Positive Selection in Independent Drosophila Lineages at the Spermatogenesis Gene roughex Genetics, June 1, 2008; 179(2): 1009 - 1020. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. E. Mank, L. Hultin-Rosenberg, E. Axelsson, and H. Ellegren Rapid Evolution of Female-Biased, but Not Male-Biased, Genes Expressed in the Avian Brain Mol. Biol. Evol., December 1, 2007; 24(12): 2698 - 2706. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Haerty, S. Jagadeeshan, R. J. Kulathinal, A. Wong, K. Ravi Ram, L. K. Sirot, L. Levesque, C. G. Artieri, M. F. Wolfner, A. Civetta, et al. Evolution in the Fast Lane: Rapidly Evolving Sex-Related Genes in Drosophila Genetics, November 1, 2007; 177(3): 1321 - 1335. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. M. Graze, O. Barmina, D. Tufts, E. Naderi, K. L. Harmon, M. Persianinova, and S. V. Nuzhdin New Candidate Genes for Sex-Comb Divergence Between Drosophila mauritiana and Drosophila simulans Genetics, August 1, 2007; 176(4): 2561 - 2576. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. E. Mank, E. Axelsson, and H. Ellegren Fast-X on the Z: Rapid evolution of sex-linked genes in birds Genome Res., May 1, 2007; 17(5): 618 - 624. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Gnad and J. Parsch Sebida: a database for the functional and evolutionary analysis of genes with sex-biased expression Bioinformatics, October 15, 2006; 22(20): 2577 - 2579. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Proschel, Z. Zhang, and J. Parsch Widespread Adaptive Evolution of Drosophila Genes With Sex-Biased Expression Genetics, October 1, 2006; 174(2): 893 - 900. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Metta, R. Gudavalli, J.-M. Gibert, and C. Schlotterer No Accelerated Rate of Protein Evolution in Male-Biased Drosophila pseudoobscura Genes Genetics, September 1, 2006; 174(1): 411 - 420. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. T. Levine, C. D. Jones, A. D. Kern, H. A. Lindfors, and D. J. Begun Novel genes derived from noncoding DNA in Drosophila melanogaster are frequently X-linked and exhibit testis-biased expression PNAS, June 27, 2006; 103(26): 9935 - 9939. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Good, C. A. Hayden, and T. J. Wheeler Adaptive Protein Evolution and Regulatory Divergence in Drosophila Mol. Biol. Evol., June 1, 2006; 23(6): 1101 - 1103. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Thornton, D. Bachtrog, and P. Andolfatto X chromosomes and autosomes evolve at similar rates in Drosophila: No evidence for faster-X protein evolution Genome Res., April 1, 2006; 16(4): 498 - 504. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. E. Popescu, T. Borza, J. P. Bielawski, and R. W. Lee Evolutionary Rates and Expression Level in Chlamydomonas Genetics, March 1, 2006; 172(3): 1567 - 1576. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Begun, H. A. Lindfors, M. E. Thompson, and A. K. Holloway Recently Evolved Genes Identified From Drosophila yakuba and D. erecta Accessory Gland Expressed Sequence Tags Genetics, March 1, 2006; 172(3): 1675 - 1681. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. J. Wagstaff and D. J. Begun Molecular Population Genetics of Accessory Gland Protein Genes and Testis-Expressed Genes in Drosophila mojavensis and D. arizonae Genetics, November 1, 2005; 171(3): 1083 - 1101. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z. Zhang and J. Parsch Positive Correlation Between Evolutionary Rate and Recombination Rate in Drosophila Genes with Male-Biased Expression Mol. Biol. Evol., October 1, 2005; 22(10): 1945 - 1947. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Begun and H. A. Lindfors Rapid Evolution of Genomic Acp Complement in the melanogaster Subgroup of Drosophila Mol. Biol. Evol., October 1, 2005; 22(10): 2010 - 2021. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. M. Hambuch and J. Parsch Patterns of Synonymous Codon Usage in Drosophila melanogaster Genes With Sex-Biased Expression Genetics, August 1, 2005; 170(4): 1691 - 1700. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Lemos, B. R. Bettencourt, C. D. Meiklejohn, and D. L. Hartl Evolution of Proteins and Gene Expression Levels are Coupled in Drosophila and are Independently Associated with mRNA Abundance, Protein Length, and Number of Protein-Protein Interactions Mol. Biol. Evol., May 1, 2005; 22(5): 1345 - 1354. [Abstract] [Full Text] [PDF]
|
|